Cited by 78Corneal surgery and disordersElasticity and Material ModelingCorneal Surgery and Treatments

Transverse depth-dependent changes in corneal collagen lamellar orientation and distribution

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Abass, Ahmed, Hayes, Sally, White, Nick, Sorensen, Thomas, Meek, Keith M.·2015·Journal of The Royal Society Interface

Abstract

It is thought that corneal surface topography may be stabilized by the angular orientation of out-of plane lamellae that insert into the anterior limiting membrane. In this study, micro-focus X-ray scattering data were used to obtain quantitative information about lamellar inclination (with respect to the corneal surface) and the X-ray scatter intensity throughout the depth of the cornea from the centre to the temporal limbus. The average collagen inclination remained predominantly parallel to the tissue surface at all depths. However, in the central cornea, the spread of inclination angles was greatest in the anterior-most stroma (reflecting the increased lamellar interweaving in this region), and decreased with tissue depth; in the peripheral cornea inclination angles showed less variation throughout the tissue thickness. Inclination angles in the deeper stroma were generally higher in the peripheral cornea, suggesting the presence of more interweaving in the posterior stroma away from the central cornea. An increase in collagen X-ray scatter was identified in a region extending from the sclera anteriorly until about 2 mm from the corneal centre. This could arise from the presence of larger diameter fibrils, probably of scleral origin, which are known to exist in this region. Incorporation of this quantitative information into finite-element models will further improve the accuracy with which they can predict the biomechanical response of the cornea to pathology and refractive procedures.

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  • Stromal interweaving in the peripheral cornea seems to extend to the deeper posterior lamellae.

    “In addition, stromal interweaving in the peripheral cornea seems to extend to the deeper posterior lamellae (Radner et al., 1998, Abass et al., 2015).”

    From Corneal structure and transparency (2015) · cites this paper as Abass et al., 2015

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  1. [1]Komai Y Ushiki T 1991 The three-dimensional organization of collagen fibrils in the human cornea and sclera. Invest. Ophthalmol. Vis. Sci. 32, 2244– 2258. 2071337
  2. [2]Radner W Zehetmayer M Aufreiter R Mallinger R 1998 Interlacing and cross-angle distribution of collagen lamellae in the human cornea. Cornea 17, 537– 543. (10.1097/00003226-199809000-00012) 9756449 · DOI · Paper page
  3. [3]Winkler M Chai D Kriling S Jy Nien C Brown DJ Jester B Juhasz T Jester JV 2011 Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics. Invest. Ophthalmol. Vis. Sci. 52, 8818– 8827. (10.1167/iovs.11-8070) 22003117 PMC3230904 · DOI
  4. [4]Winkler M Shoa G Xie Y Petsche SJ Pinsky PM Juhasz T Brown DJ Jester JV 2013 Three-dimensional distribution of transverse collagen fibers in the anterior human corneal stroma. Invest. Ophthalmol. Vis. Sci. 54, 7293– 7301. (10.1167/iovs.13-13150) 24114547 PMC4589141 · DOI · Paper page
  5. [5]Kohlhaas M Spoerl E Schilde T Unger G Wittig C Pillunat LE 2006 Biomechanical evidence of the distribution of cross-links in corneas treated with riboflavin and ultraviolet A light. J. Cataract Refract. Surg. 32, 279– 283. (10.1016/j.jcrs.2005.12.092) 16565005 · DOI
  6. [6]Randleman JB Woodward M Lynn MJ Stulting RD 2008 Risk assessment for ectasia after corneal refractive surgery. Ophthalmology 115, 37– 50. (10.1016/j.ophtha.2007.03.073) 17624434 · DOI
  7. [7]Petsche SJ Chernyak D Martiz J Levenston ME Pinsky PM 2012 Depth-dependent transverse shear properties of the human corneal stroma. Invest. Ophthalmol. Vis. Sci. 53, 873– 880. (10.1167/iovs.11-8611) 22205608 PMC3317426 · DOI
  8. [8]Müller LJ Pels E Vrensen GFJM 2001 The specific architecture of the anterior stroma accounts for maintenance of corneal curvature. Br. J. Ophthalmol. 85, 437– 443. (10.1136/bjo.85.4.437) 11264134 PMC1723934 · DOI · Paper page
  9. [9]Morishige N Wahlert AJ Kenney MC Brown DJ Kawamoto K Chikama T Nishida T Jester JV 2007 Second-harmonic imaging microscopy of normal human and keratoconus cornea. Invest. Ophthalmol. Vis. Sci. 48, 1087– 1094. (10.1167/iovs.06-1177) 17325150 PMC1894888 · DOI
  10. [10]Meek KM Boote C 2009 The use of X-ray scattering techniques to quantify the orientation and distribution of collagen in the corneal stroma. Prog. Retin. Eye Res. 28, 369– 392. (10.1016/j.preteyeres.2009.06.005) 19577657 · DOI
  11. [11]Meek KM Quantock AJ 2001 The use of X-ray scattering techniques to determine corneal ultrastructure. Prog. Retin. Eye Res. 20, 95– 137. (10.1016/S1350-9462(00)00016-1) 11070369 · DOI · Paper page
  12. [12]Daxer A Fratzl P 1997 Collagen fibril orientation in the human corneal stroma and its implication in keratoconus. Invest. Ophthalmol. Vis. Sci. 38, 121– 129. 9008637
  13. [13]Meek K Blamires T Elliot G Gyi TJ Nave C 1987 The organisation of collagen fibrils in the human corneal stroma: a synchrotron X-ray diffraction study. Curr. Eye Res. 6, 841– 846. (10.3109/02713688709034853) 3621979 · DOI · Paper page
  14. [14]Meek K Elliot GE Hughes RA Nave C 1983 The axial density in collagen fibrils from human corneal stroma. Curr. Eye Res. 2, 471– 477. (10.3109/02713688208996351) 7182107 · DOI
  15. [15]Newton RH Meek KM 1998 The integration of the corneal and limbal fibrils in the human eye. Biophys. J. 75, 2508– 2512. (10.1016/S0006-3495(98)77695-7) 9788946 PMC1299925 · DOI
  16. [17]Abahussin M Hayes S Knox Cartwright NE Kamma-Lorger CS Khan Y Marshall J Meek KM 2009 3D collagen orientation study of the human cornea using X-ray diffraction and femtosecond laser technology. Invest. Ophthalmol. Vis. Sci. 50, 5159– 5164. (10.1167/iovs.09-3669) 19516010 · DOI · Paper page
  17. [18]Quantock AJ 2007 Small-angle fibre diffraction studies of corneal matrix structure: a depth-profiled investigation of the human eye-bank cornea. J. Appl. Crystallogr. 40, 335– 340. (10.1107/S0021889807005523) · DOI
  18. [19]Boote C Hayes S Abahussin M Meek K 2006 Mapping collagen organisation in the human cornea: left and right eyes are structurally distinct. Invest. Ophthalmol. Vis. Sci. 47, 901– 908. (10.1167/iovs.05-0893) 16505022 · DOI · Paper page
  19. [20]Meek KM 2009 Corneal collagen—its role in maintaining corneal shape and transparency. Biophys. Rev. 1, 83– 93. (10.1007/s12551-009-0011-x) 28509987 PMC5425665 · DOI · Paper page
  20. [21]Garcia D 2010 Robust smoothing of gridded data in one and higher dimensions with missing values. Comput. Stat. Data Anal. 54, 1167– 1178. (10.1016/j.csda.2009.09.020) 24795488 PMC4008475 · DOI
  21. [22]Fratzl P Daxer A 1993 Structural transformation of collagen fibrils in the corneal stroma during drying: an X-ray scattering study. Biophys. J. 64, 1210– 1214. (10.1016/S0006-3495(93)81487-5) 8494978 PMC1262438 · DOI
  22. [23]Meek KM Fullwood NJ Cooke PH Elliott GF Maurice DM Quantock AJ Wall RS Worthington CR 1991 Synchrotron X-ray-diffraction studies of the cornea, with implications for stromal hydration. Biophys. J. 60, 467– 474. (10.1016/S0006-3495(91)82073-2) 1912282 PMC1260084 · DOI
  23. [24]Malik NS Moss SJ Ahmed N Furth AJ Wall RS Meek KM 1992 Aging of the human corneal stroma—structural and biochemical changes. Biochim. Biophys. 1138, 222– 228. (10.1016/0925-4439(92)90041-K) 1547284 · DOI
  24. [25]Hayes S Boote C Tuft SJ Quantock AJ Meek KM 2007 A study of corneal thickness, shape and collagen organisation in keratoconus using videokeratography and X-ray scattering techniques. Exp. Eye Res. J. 84, 423– 434. (10.1016/j.exer.2006.10.014) 17178118 · DOI
  25. [26]Fullwood NJ Tuft SJ Malik NS Meek KM Ridgway AEA Harrison RJ 1992 Synchrotron X-ray diffraction studies of keratoconus corneal stroma. Invest. Ophthalmol. Vis. Sci. 33, 1734– 1741. 1559773
  26. [27]Read SA Collins MJ Carney LG Franklin RJ 2006 The topography of the central and peripheral cornea. Invest. Ophthalmol. Vis. Sci. 47, 1404– 1415. (10.1167/iovs.05-1181) 16565374 · DOI
  27. [28]Ho L Sigal I Jan N Squires A Tse Z Wu E Kim S-G Schuman JS Chan KC 2014 Magic angle-enhanced MRI of fibrous microstructures in sclera and cornea with and without intraocular pressure loading. Invest. Opthalmol. Vis. Sci. 55, 5662– 5672. (10.1167/iovs.14-14561) PMC4160095 25103267 · DOI
  28. [29]Liu X 2014 A mechanical model of the cornea considering the crimping morphology of collagen fibrils. Invest. Ophthalmol. Vis. Sci. 55, 2739– 2746. (10.1167/iovs.13-12633) 24692124 · DOI
  29. [30]Polack FM 1961 Morphology of the cornea. Am. J. Ophthalmol. 51, 179– 184. (10.1016/0002-9394(61)91794-9) 13736666 · DOI · Paper page
  30. [31]Dua HS Faraj LA Said DG Gray T Lowe J 2013 Human corneal anatomy redefined: a novel pre-Descemet's layer (Dua's layer). Ophthalmology 120, 1778– 1785. (10.1016/j.ophtha.2013.01.018) 23714320 · DOI · Paper page
  31. [32]Hayashi S Osawa T Tohyama K 2002 Comparative observations on corneas, with special reference to Bowman's layer and Descemet's membrane in mammals and amphibians. J. Morphol. 254, 247– 258. (10.1002/jmor.10030) 12386895 · DOI
  32. [34]Grewal S Laibson PR Cohen EJ Rapuano CJ 1999 Acute hydrops in the corneal ectasias: associated factors and outcomes. Trans. Am. Ophthalmol. Soc. 97, 187– 203. 10703124 PMC1298260
  33. [35]Jafarinasab M Rahmati-Kamel M Rezaei Kanavi M Feizi S 2010 Dissection plane in deep anterior lamellar keratoplasty using the big-bubble technique. Cornea 29, 388– 391. (10.1097/ICO.0b013e3181ca324c) 20164750 · DOI
  34. [36]Basu S Vaddavalli PK Vemuganti GK Ali H Murthy SI 2012 Anterior segment optical coherence tomography features of acute corneal hydrops. Cornea 31, 479– 485. (10.1097/ICO.0b013e318223988e) 22314821 · DOI
  35. [37]Castoro JA Bettelheim AA Bettleheim FA 1988 Water gradients across the bovine cornea. Invest. Ophthalmol. Vis. Sci. 29, 963– 968. 3131266
  36. [38]Akhtar S Bron A Salvi S Hawksworth N Tuft S Meek K 2008 Ultrastructural analysis of collagen fibrils and proteoglycans in keratoconus. Acta Ophthalmol. 86, 764– 772. (10.1111/j.1755-3768.2007.01142.x) 18422999 · DOI
  37. [39]Kamma-Lorger CS 2010 Collagen and mature elastic fibre organisation as a function of depth in the human cornea and limbus. J. Struct. Biol. 169, 424– 430. (10.1016/j.jsb.2009.11.004) 19914381 · DOI · Paper page
  38. [40]Boote C 2009 Ultrastructural changes in the retinopathy, globe enlarged (rge) chick cornea. J. Struct. Biol. 166, 195– 204. (10.1016/j.jsb.2009.01.009) 19258040 PMC2680986 · DOI · Paper page
  39. [41]Hjortdal JO 1996 Regional elastic performance of the human cornea. J. Biomech. 29, 931– 942. (10.1016/0021-9290(95)00152-2) 8809623 · DOI
  40. [42]Pinsky PM van der Heide D Chernyak D 2005 Computational modeling of mechanical anisotropy in the cornea and sclera. J. Cataract Refract. Surg. 31, 136– 145. (10.1016/j.jcrs.2004.10.048) 15721706 · DOI
  41. [43]Li LY Tighe B 2006 The anisotropic material constitutive models for the human cornea. J. Struct. Biol. 153, 223– 230. (10.1016/j.jsb.2005.10.014) 16426861 · DOI
  42. [44]Pandolfi A Holzapfel GA 2008 Three-dimensional modeling and computational analysis of the human cornea considering distributed collagen fibril orientations. J. Biomech. Eng. 130, 061006 (10.1115/1.2982251) 19045535 · DOI
  43. [45]Studer H Larrea X Riedwyl H Buchler P 2010 Biomechanical model of human cornea based on stromal microstructure. J. Biomech. 43, 836– 842. (10.1016/j.jbiomech.2009.11.021) 20006338 · DOI
  44. [46]Petsche SJ Pinsky PM 2013 The role of 3-D collagen organization in stromal elasticity: a model based on X-ray diffraction data and second harmonic-generated images. Biomech. Model. Mechanobiol. 12, 1101– 1113. (10.1007/s10237-012-0466-8) 23288406 · DOI

Cited by

Sorted by citations

Authors
Abass, A., Hayes, S., White, N., Sorensen, T., & Meek, K. M.
Affiliations
  • Cardiff University (GB)
  • Diamond Light Source Ltd, Diamond House, Harwell Science and Innovation Campus, Didcot, Oxfordshire OX11 0DE, UK
Corresponding author
Meek, Keith M.
Venue
Journal of The Royal Society Interface
Published
2015-03
Volume
12
Issue
104
Pages
20140717
ISSN
  • 1742-5662 (ISSN-L)
  • 1742-5689
OpenAlex
W2102640190
Cited by
78
References
1
Citations by year
2026: 7 · 2025: 8 · 2024: 5 · 2023: 14 · 2022: 5 · 2021: 9 · 2020: 4 · 2019: 7 · 2018: 5 · 2017: 5 · 2016: 6 · 2015: 3
FWCI
4.67
Type
journal article
Language
en
Open access
Locations
  • Journal of The Royal Society Interface (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
Funders
  • Diamond Light Source
  • National Institute for Health and Care Research (503626)
  • Medical Research Council (MR/K000837/1, 503626)
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Corneal surgery and disorders
  • Physical Sciences › Engineering › Biomedical Engineering › Elasticity and Material Modeling
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Corneal Surgery and Treatments
Keywords
corneal collagen, collagen lamellae, lamellar orientation, corneal stroma, corneal biomechanics, finite element model, corneal limbus, corneal thickness
MeSH terms
Aged, Aged, 80 and over, Biomechanical Phenomena, Collagen, Cornea, Female, Humans, Male, Membranes, Artificial, Middle Aged, Radiography, Scattering, Radiation, Sclera, X-Ray Diffraction, X-Rays, Corneal Topography

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